Helgol Mar Res (2012) 66:621–634 DOI 10.1007/s10152-012-0296-1

ORIGINAL ARTICLE

Mesozooplankton and community structures in the southern East China Sea: the status during the monsoonal transition period in September

Li-Chun Tseng • Hans-Uwe Dahms • Qing-Chao Chen • Jiang-Shiou Hwang

Received: 14 April 2011 / Revised: 4 February 2012 / Accepted: 10 February 2012 / Published online: 25 February 2012 Ó Springer-Verlag and AWI 2012

Abstract A field sampling was conducted before the onset and comprising about 50% of all amphipods. Chaetognath of the northeasterly monsoon to investigate the copepod abundance showed a significantly negative correlation with community composition during the monsoon transition salinity (r = 0.77, p = 0.027), whereas mesozooplankton period at the northern coast of Taiwan (East China Sea). In group numbers had a significantly positive correlation with total, 22 major mesozooplankton taxa were found, with the salinity (r = 0.71, p = 0.048). Densities of four copepod (relative abundance: 66.36%) and ( sinicus, pavo, Calanopia (9.44%) being the most abundant. Mesozooplankton densi- elliptica and Labidocera acuta) showed a significantly neg- ties ranged between 226.91 and 2162.84 individuals m-3 ative correlation with temperature. Communities of (mean ± SD: 744.01 ± 631.5 individuals m-3). A total of mesozooplankton and of northern Taiwan varied 49 copepod species were identified, belonging to 4 orders, 19 spatially with the distance to land. The results of this study families, and 30 genera. The most abundant species were: provide evidence for the presence of C. sinicus in the coastal turbinata (23.50%), Undinula vulgaris (17.92%), area of northern Taiwan during the early northeast monsoon and Acrocalanus gibber (14.73%). The chaetognath Flacc- transition period in September. isagitta enflata occurred at all 8 sampling stations, providing a 95% portion of the overall chaetognath contribution. Keywords Mesozooplankton Copepod Amphipoda were abundant at stations 4 and 5, with Hype- East China Sea Monsoon transition period rioides sibaginis and Lestigonus bengalensis being dominant,

Introduction Communicated by Heinz-Dieter Franke. The marine biota in the waters around the island of Taiwan Li-Chun Tseng and Hans-Uwe Dahms are contributed equally to the is highly diverse. It has been estimated that around 10% of present contribution. the world’s marine species can be found in waters around L.-C. Tseng J.-S. Hwang (&) Taiwan (Shao 1998). Several authors explained this high Institute of Marine Biology, National Taiwan Ocean University, biodiversity as being caused by the convergence of several 2 Pei-Ning Road, Keelung 20224, Taiwan large water masses (Jan et al. 2002; Hwang et al. 2010a; e-mail: [email protected] Tseng et al. 2011a). Copepod communities in Taiwan L.-C. Tseng waters are highly influenced by water masses from ocean e-mail: [email protected] currents (Hwang et al. 2004, 2006, 2010b; Dur et al. 2007; H.-U. Dahms Tseng et al. 2008b, d, e; Lan et al. 2009). Temperate Green Life Science Department, College of Convergence, species are transferred from the north and tropical species Sangmyung University, Seoul 110-743, Korea from the south via the Taiwan Strait, affecting the meso- communities on the west coast of Taiwan Q.-C. Chen South China Sea Institute of Oceanology, (Hwang et al. 2004, 2006, 2009; Dur et al. 2007; Tseng Chinese Academy of Science, Guangzhou, China et al. 2008a, e). 123 622 Helgol Mar Res (2012) 66:621–634

The Kuroshio Current flows from the equator via the Table 1 Locations and dates/day times of sampling on cruise ORII- east coast of the Philippines and brings warm water masses CR488 (2–3/September/1998) all along the east coast of Taiwan year round. In this Station Latitude Longitude Date manner, many warm water species from the south reach the (N) (E) (September/day time) western and northern coastal areas of Taiwan (Hsiao et al. 125°09.8090 121°46.5200 02/18:04 2004; Hwang et al. 2007; Tseng et al. 2008a, b, e). In the 225°14.9570 121°40.3550 02/19:17 Taiwan Strait and at the southern edge of the East China 325°21.7170 121°47.0540 02/20:59 Sea (ECS), water circulation is strongly influenced by the 425°27.6660 121°52.1050 02/22:32 prevailing monsoonal winds and their seasonal changes 525°33.5460 121°58.4690 03/00:25 (Lee and Chao 2003; Tseng et al. 2008b). During the 0 0 northeast (NE) monsoon period in winter and spring 625°39.874 122°04.830 03/02:00 0 0 (September to March), the China Coastal Current (CCC) 725°45.529 122°10.716 03/03:48 0 0 brings cold water masses from the Bohai Sea, the Yellow 825°51.256 122°16.918 03/06:00 Sea and the ECS to the Taiwan Strait (Wong et al. 2000; Liang et al. 2003; Lo et al. 2004a; Zuo et al. 2006; Tseng Taiwan. The sampling stations included one station near et al. 2008b). The southwest (SW) monsoon brings species Bi-Sar Harbor (northern Taiwan) and seven stations located from the South China Sea during summer and autumn on the transect between northern Taiwan and Pengjiayu Island (April to August) to the south of Taiwan (Lo et al. 2001; in the southern ECS, between 25°09.8090–25°51.2560Nand Liao et al. 2006; Tseng et al. 2008b; Lan et al. 2004, 2009). 121°40.3550–122°16.9180E(Table1, Fig. 1). Such complex water exchange affects the composition A research cruise was conducted in September 1998, i.e. and abundance of oceanic biota around the island of before the onset of the northeasterly monsoon. Zooplankton Taiwan. This also holds for microzooplankton (Vandromme samples were collected at the 8 selected stations by surface et al. 2010; Chang et al. 2011) and the mesozooplankton tows (0–5 m) with a standard North Pacific zooplankton net dominated by copepods (Liao et al. 1999; Tseng et al. (mouth diameter 45 cm, mesh size 333 lm) provided with a 2008e). Pelagic copepods are important food sources for fish flow meter in the center of the net opening (Hydrobios; Kiel, (Dahms and Hwang 2007; Mahjoub et al. 2011) and likely Germany). Samples were preserved immediately in 5% buf- play a pivotal role in the transfer of matter and energy in the fered formaldehyde in seawater. Prior to collection, southern Taiwan Strait (Tseng et al. 2008c) and in the salinity and temperature were measured on board. In the northern South China Sea (Tseng et al. 2009). laboratory, samples were split by a Folsom splitter until the Zooplankton communities have long been applied as subsample contained less than 500 specimens. Copepods and indicators of water movements (Hwang and Wong 2005; mesozooplankton were sorted and identified at the species Dahms and Hwang 2010). In northern Taiwan, long-term level using the identification aids of Chen and Zhang (1965), studies of copepod successions showed that Calanus sinicus is Chen et al. (1974) and Chihara and Murano (1997). Additional an important indicator species for cold water masses from the original papers were used for species identification if required. Bohai Sea and the Yellow Sea (Hwang et al. 2004, 2006;Dur et al. 2007). Hwang et al. (2004)describedC. sinicus as rare in Statistical analyses samples from July to September, but the species appeared again in October, dramatically increasing in density and Species density matrices were analyzed using multivariate occurrence ratio. As yet, however, it is not known when analyses for copepod species. Non-metric cluster analysis exactly C. sinicus reaches the coastal areas of northern Taiwan was performed together with the Bray–Curtis similarity from the north. The present study aimed to characterize the index after logarithmic transformations of species abun- mesozooplankton community and copepod assemblages dance data. Significance levels of copepod assemblages during the southwest (SW)–northeast (NE) monsoon transi- between stations were calculated using a similarity pro- tion period in northern Taiwan waters because this appears to gram provided by the Plymouth Routine in Multivariate be an important period for community alterations. Ecological Research (PRIMER), version IV software package (Clarke and Warwick 1994). The abundance of copepod species of whole samples were used for the cal- Materials and methods culation of similarities before clustering. The functional test of Box and Cox (1964) for the transformation of data Field sampling was applied before the similarity analysis. The value (k)of the power transformation was set as 0.95, and the log For the present study, we selected the coastal waters of the (x ? 1) was applied to treat the individual densities of all southern ECS in the vicinity of Taipei County of northern samples. 123 Helgol Mar Res (2012) 66:621–634 623

Fig. 1 Map of the sampling stations on cruise ORII-CR488 during 2–3/September/1998

The copepod species characterizing each cluster were the IndVal indices. To evaluate copepod assemblages for further identified using the Indicator Value Index (IndVal) the present sampling period, an analysis of indicator spe- proposed by Dufreˆne and Legendre (1997). This index is cies was applied to each sampling cruise separately. obtained by multiplying the product of two independently The Shannon-Wiener diversity index was used to eval- computed values by 100: uate species diversity, and Pielou’s evenness was used to IndValðj; sÞ¼100SPðj; sÞFIðj; sÞ measure the relative abundance of species at each station. The relationship between copepod abundance and tem- where (SPj, s) is the specificity, and (FIj, s) is the fidelity of perature and salinity was studied with Pearson’s product a species (s) towards a group of samples (j), and these are moment correlation. calculated by: NIðj; sÞ NSðj; sÞ SPðj; sÞ¼ ; FIðj; sÞ¼ Results RNIðsÞ RNSðsÞ where NI(j, s) is the mean abundance of species s across Hydrographic and weather conditions samples pertaining to j, RNI(s) is the sum of the mean abundances of species s within the various groups in the In September 1998, the monthly-averaged sea surface partition, NS(j, s) is the number of samples in j where temperature (SST; satellite images from NOAA) in the area species s is present, and RNS(s) is the total number of north of Taiwan showed values higher than 28°C (Fig. 2). samples in that group. The specificity of a species for a In northeastern Taiwan (southern ECS), where water group is greatest if a species is present only in a particular masses are derived from the Kuroshio Current flowing group, whereas the fidelity of a species to a group is along the eastern Philippines, the surface waters in greatest if the species is present in all samples of the group September 1998 had temperatures even higher than 30°C. considered. Here, we only considered values of SP(j, s) In the area of the northern Taiwan Strait, the CCC brings above 5% of each cluster grouping for the calculation of colder waters from the ECS into the Taiwan Strait, and the

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Fig. 2 Satellite image showing the monthly-averaged surface seawater temperature in September 1998

water temperatures were about 26–27°C. The slight varia- Transportation and Communications, Taiwan. Keelung tions in salinity and water temperature among stations are City is located in northeastern Taiwan adjacent to the shown in Fig. 3a. The water temperature at a depth of 5 m sampling area. During the recording period, the daily ranged from 26.75°C (station 5) to 28.56°C (station 1); average temperature varied from 17.2°C (11/December) to the average temperature of all sampling stations was 32.6°C (20/July). The air temperature in summer (July and 27.85 ± 0.59°C. The salinity at a depth of 5 m ranged August) was higher than 29.0°C (Fig. 4a). The temperature between 33.49 (station 2) and 34.19 (station 7) (Fig. 3b). The showed a decreasing trend from July to the end of 1998. average salinity of all sampling stations was 33.77 ± 0.28. The wind direction followed the monsoonal changes (0 and The salinities were lowest at stations 1 and 2 of the coastal 360 degree means wind coming from the north, 90 degree area and showed an increase with distance to the coastline of means wind from the east, etc.) (Fig. 4b). The SW mon- Taiwan (particularly at stations 3 to 8). The salinity variation soon prevails in summer (July to mid-September) and the among stations was affected by freshwater from the island NE monsoon from mid-September to the end of December. mixed with waters of the Kuroshio Current (Fig. 2). A During the SW monsoon period air temperatures were temperature-salinity diagram characterizes the water masses higher than during the NE monsoon period. A transition at each sampling station (Fig. 3b). The similarities in the period occurred during September. Most records of wind temperature/salinity profiles indicate that waters at all sam- direction before September belonged to the SW monsoon pling stations belonged to the same water mass. and this changed during the NE monsoon after September. Figure 4 shows the daily averages (recorded every hour) The daily average wind speed varied from 1.1 to 7.5 ms-1. of air temperature, wind direction, and wind speed from Both lowest (October 21 and December 21) and highest 1/July/1998 to the 1/January/1999. Data were retrieved (October 16) wind speeds were recorded, when the NE from the automatic monitoring instrument of the Cen- monsoon prevailed (Fig. 4c). Wind speeds during the SW tral Weather Bureau at Keelung City, Ministry of monsoon period were lower than 6 ms-1 before 123 Helgol Mar Res (2012) 66:621–634 625

(a) 29 35 34.2 Salinity (a) Air temperature C)

Temperature o

30

34.0 28 C) o

33.8 25

Salinity 27

33.6

Temperature ( 20 Seawater temperature ( 33.4 26 12345678 15 Station 360 30 N (b) (b) Wind direction

28 270 W C)

o 26 180 S

24 St 1 90 E St 2 22 St 3 St 4 Wind direction (360 degree) St 5 0 N 20 St 6

Seawater temperature ( St 7 8 St 8 (c) Wind speed 18 )

-1 6 16 33.2 33.4 33.6 33.8 34.0 34.2 34.4 34.6 Salinity 4

Fig. 3 Temperature and salinity at 10 m depth at the sampling stations 1–8 2 Wind speed (m sec.

0 September. The daily variations in wind speed records Jul/1998 Aug Sep Oct Nov Dec Jan/1999 were higher during the period of the NE monsoon (Fig. 4c) Period from September onwards. Fig. 4 Air temperature (a), wind direction (b) and wind speed (c) during the period from 1/July/1998 to the 1/January/1999 Mesozooplankton composition and abundance (information from the automatic monitoring instrument of the Central Weather Bureau at Keelung City, Ministry of Transportation and Among the samples from the 8 stations, we identified 22 Communications, Taiwan) mesozooplankton groups (Table 2). The numerically dominant groups were calanoid copepods (relative abun- lowest temperature of all stations. The numbers of meso- dance 66.36%) and chaetognaths (9.44%), which together zooplankton group ranged between 7 (station 3) and 18 comprised 75.80% of the overall mesozooplankton counts (station 6) station-1, averaging 13.25 ± 3.92 station-1. (Table 2). Figure 5 shows, for each sampling station, total Thus, station 6 showed the lowest mesozooplankton den- abundance and number of groups (Fig. 5a) as well as the sity, but the highest group number in this sampling cruise. proportions of the six top dominant groups (Fig. 5b). Both There was no correlation between density and number of total abundance values and numbers of groups varied groups (r =-0.410, p = 0.313, Pearson’s correlation). clearly among stations. The mesozooplankton densities Five mesozooplankton groups were dominant in the present ranged between 226.9 (station 6) and 2162.8 (station 5) study: Calanoida, Chaetognatha, other Decapoda (i.e. individuals m-3, and the average was 744.0 ± 631.5 decapods except of Lucifer larvae, Table 2), Poecilosto- individuals m-3. Station 5 showed the highest density matoida and Amphipoda (Fig. 5b). At all sampling sta- values of mesozooplankton, which correlated with the tions, calanoid copepods were the most dominant group,

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Table 2 Abundance (mean ± SD), relative abundance (RA) and (a) 2500 20 occurrence ratio (OR) of each mesozooplankton group recorded on Density cruise ORII-CR488 (2–3/September/1998) 2000 Group no. 16 ) Group Abundance RA OR -3 (individuals m-3) (%) (%) 1500 12 Medusae 3.2 ± 5.85 0.43 62.5 1000

Polychaeta 1.45 ± 2.97 0.19 50.0 Group number

(Individuals m (Individuals 8 Sagitta spp. 70.23 ± 49.6 9.44 100.0 500 Mesozooplankton density Mesozooplankton Cladocera 0.64 ± 1.49 0.09 25.0 0 4 Ostracoda 0.61 ± 1.48 0.08 37.5 Copepod nauplii 0.03 ± 0.08 0.00 12.5 (b) Calanoida Chaetognatha Calanoida 493.74 ± 450.54 66.36 100.0 Other Decapoda Poecilostomatoida Amphipoda Other groups 0.56 ± 1.49 0.07 25.0 100 0.03 ± 0.08 0.00 12.5 80 Poecilostomatoida 23.61 ± 27.49 3.17 100.0

Amphipoda 22.32 ± 55.57 3.00 50.0 60 Lucifer larvae 12.71 ± 12.74 1.71 87.5 Euphausiacea 0.82 ± 1.22 0.11 37.5 40 Mysidacea 1.99 ± 3.01 0.27 50.0 20 Other Decapoda 49.45 ± 77.32 6.65 75.0 Stacked percentages (%)

Pteropoda 21.47 ± 15.43 2.89 100.0 0 larvae 0.75 ± 1.3 0.10 37.5 12345678 Appendicularia 8.34 ± 13.23 1.12 75.0 Sampling station Thaliacea 11.24 ± 8.4 1.51 100.0 Fig. 5 Mesozooplankton recorded at stations 1–8; a mesozooplankton eggs 1.17 ± 1.62 0.16 50.0 density and numbers of mesozooplankton groups; b relative abundance Fish larvae 1.29 ± 1.6 0.17 50.0 (proportion) of the 6 most dominant groups Other larvae 18.38 ± 28.31 2.47 87.5 total mesozooplankton abundance (r = 0.999, p \ 0.001, with a contribution ranging from 42.99% (station 6) to Pearson’s correlation), indicating that calanoid copepods 78.39% (station 8). Decapods showed higher abundance were the dominant group of mesozooplankton in the values at stations 4, 5 and 6, with contributions of 30.77%, southern ECS during the monsoon transition period. 7.75% and 13.18%, respectively (Fig. 5b). Chaetognaths were identified at all eight sampling stations. The dominant Copepod diversity and abundance species was Flaccisagitta enflata (Grassi 1881), amounting to 95% of all chaetognath samples. The second most From the 8 stations, we identified 49 copepod species. abundant species was Serratosagitta pacifica (Tokioka They belonged to 4 orders, 19 families, and 30 genera 1940) (2–3%), and other species were Ferosagitta ferox (Table 3). Figure 6 shows the variation in copepod abun- (Doncaster 1902), F. robusta (Doncaster 1902), Mesosa- dance and species number (Fig. 6a), as well as in species gitta minima (Grassi 1881), Decipisagitta decipiens richness, diversity index and evenness index (Fig. 6b) (Fowler 1905), Aidanosagitta delicate (Tokioka 1939), A. among sampling stations. Total copepod densities ranged neglecta (Aida 1897), and A. regularis (Aida 1897), with a between 110.24 (station 6) and 1567.64 (station 5) indi- relative abundance of around 2–3% of the chaetognath viduals m-3, with a mean of 517.94 ± 470.02 individuals samples (Fig. 5b). Amphipoda were abundant at stations 4 m-3. It showed a similar variation over the sampling sta- and 5. The two most abundant amphipod species were tions as total mesozooplankton abundance, with highest represented by Hyperioides sibaginis (Stebbing 1888) and values at station 5, where surface temperature was lowest. Lestigonus bengalensis Giles 1887; they had a relative The copepod species numbers ranged between 16 (stations abundance of around 50% of the amphipod samples, fol- 1 and 2) and 34 (station 8), with a mean of 21.38 ± 6.37 lowed by Lestrigonus schizogeneios (Stebbing 1888) with species station-1 (Fig. 6a). Copepod densities showed no 21%. Other amphipods belonging to the genera Lestrig- clear trend over the sampling stations (r =-0.225, onus, Hyperioides and Hyperietta showed a contribution of p = 0.592, Pearson’s correlation), but the species number around 20% to the amphipod samples (Fig. 5b). The den- increased significantly with the distance from the coastline sities of calanoid copepods were positively correlated with of Taiwan (r = 0.875, p = 0.004, Pearson’s correlation).

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Table 3 Abundance Species Abundance RA OR (mean ± SD), relative (individuals m-3) (%) (%) abundance (RA) and occurrence ratio (OR) of each copepod Calanoida species recorded on cruise ORII-CR488 (2–3/September/ Acartiidae 1998) Acartia(Odontacartia) erythraea Giesbrecht 1889 0.11 ± 0.30 0.02 12.50 Acartia(Plantacartia) negligens Dana 1849 0.87 ± 2.29 0.17 25.00 Calanidae Calanus sinicus Brodsky 1965 3.37 ± 5.72 0.65 50.00 Canthocalanus pauper (Giesbrecht) 1888 59.52 ± 49.02 11.49 100.00 Cosmocalanus darwini (Lubbock) 1860 2.02 ± 2.99 0.39 50.00 Nannocalanus minor (Claus) 1863 3.95 ± 8.92 0.76 37.50 Undinula vulgaris (Dana) 1849 92.8 ± 85.44 17.92 100.00 Calocalanidae Calocalanus pavo (Dana) 1849 2.9 ± 3.42 0.56 62.50 Calocalanus plumulosus (Claus) 1863 0.03 ± 0.08 0.01 12.50 Candaciidae Candacia bradyi A. Scott 1902 0.95 ± 1.83 0.18 25.00 Candacia catula (Giesbrecht) 1889 0.27 ± 0.76 0.05 12.50 Candacia ethiopica (Dana) 1849 0.05 ± 0.15 0.01 12.50 Paracandacia truncata (Dana) 1849 0.56 ± 1.49 0.11 25.00 Centropagidae Centropages furcatus (Dana) 1849 10.55 ± 17.24 2.04 87.50 Centropages orsini Giesbrecht 1889 0.56 ± 1.00 0.11 37.50 Clausocalanidae Clausocalanus arcuicornis (Dana) 1849 9.81 ± 15.4 1.89 50.00 Clausocalanus furcatus (Brady) 1883 0.51 ± 1.15 0.10 25.00 Clausocalanus mastigophorus (Claus) 1863 0.26 ± 0.52 0.05 25.00 Eucalanidae Pareucalanus attenuatus (Dana) 1849 0.56 ± 1.49 0.11 25.00 Rhincalanus rostrifrons (Dana) 1852 0.03 ± 0.08 0.01 12.50 Subeucalanus crassus (Giesbrecht) 1888 0.03 ± 0.08 0.01 12.50 Subeucalanus subcrassus (Giesbrecht) 1888 21.61 ± 20.43 4.17 100.00 Euchaetidae Euchaeta indica Wolfenden 1905 0.35 ± 0.98 0.07 12.50 Euchaeta plana Mori 1937 2.25 ± 3.52 0.43 37.50 Euchaeta rimana Bradford 1973 0.18 ± 0.51 0.03 12.50 Lucicutiidae Lucicutia flavicornis (Claus) 1863 0.15 ± 0.42 0.03 12.50 Metridinidae Pleuromamma gracilis (Claus) 1863 0.2 ± 0.56 0.04 12.50 Paracalanidae Acrocalanus gibber Giesbrecht 1888 76.29 ± 130.81 14.73 87.50 Acrocalanus gracilis Giesbrecht 1888 38.35 ± 32.48 7.40 100.00 Acrocalanus monachus Giesbrecht 1888 0.97 ± 1.49 0.19 50.00 Paracalanus parvus (Claus) 1863 3.52 ± 4.20 0.68 87.50 Pontellidae Calanopia elliptica (Dana) 1849 7.09 ± 11.05 1.37 75.00 Calanopia minor A. Scott 1902 10.32 ± 13.02 1.99 87.50 Labidocera acuta (Dana) 1849 8.46 ± 17.45 1.63 50.00 Labidocera minuta Giesbrecht 1889 0.41 ± 1.15 0.08 12.50 Pontellina plumata (Dana) 1849 1.05 ± 2.96 0.20 12.50

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Table 3 continued Species Abundance RA OR (individuals m-3) (%) (%)

Scolecithricidae Scolecithrix danae (Lubbock) 1856 0.58 ± 1.49 0.11 25.00 Temora discaudata (Giesbrecht) 1889 10.54 ± 23.46 2.03 62.50 Temora turbinata (Dana) 1849 121.71 ± 148.08 23.50 100.00 Cyclopoida Oithonidae Oithona setigera (Dana) 1849 0.56 ± 1.49 0.11 25.00 Harpacticoida Miraciidae Macrosetella gracilis (Dana) 1847 0.03 ± 0.08 0.01 12.50 Poecilostomatoida Corycaeus(Corycaeus) speciosus Dana 1849 1.04 ± 1.70 0.20 50.00 Corycaeus(Ditrichocorycaeus) asiaticus F. Dahl 1894 0.15 ± 0.42 0.03 12.50 Corycaeus(Ditrichocorycaeus) dahli Tanaka 1957 1.01 ± 1.59 0.20 37.50 Corycaeus(Farranula) gibbula Giesbrecht 1891 2.34 ± 3.00 0.45 50.00 Corycaeus(Onychocorycaeus) pumilus M. Dahl 1912 1.17 ± 1.69 0.23 50.00 venusta Philippi 1843 16.22 ± 23.22 3.13 87.50 mirabilis Dana 1849 1.66 ± 2.89 0.32 62.50 nigromaculata Claus 1863 0.03 ± 0.08 0.01 12.50

The copepod species richness, Shannon-Wiener diver- 1600 40 (a) sity and evenness indices differed among sampling stations Density 35 (Fig. 6b). The richness index ranged from 1.11 (station 1) 1200 Species no. ) to 2.75 (station 8), and the average value was 1.61 ± 0.57. -3 30 The evenness index ranged between 0.6 (station 8) and 800 25 0.84 (station 4 and 7), with a mean of 0.72 ± 0.09. The

20 Shannon-Wiener diversity index ranged from 1.74 (station

400 Species number 2) to 2.76 (station 7), with a mean value of 2.71 ± 0.30. (Individuals m Copepod density 15 Richness index and species number showed a similar trend,

0 10 increasing with the distance from the coast. The richness index showed a significant positive correlation (r = 0.98, 3.0 1.0 (b) Richness index p \ 0.001, Pearson’s correlation) with species number. The Diversity Index evenness and Shannon-Wiener diversity indices did not Pielou's evenness index 0.9 2.5 show a clear trend, but were positively correlated with each 0.8 other (r = 0.785, p = 0.021, Pearson’s correlation). 2.0 The most common copepod species in the present study 0.7 were: Acrocalanus gracilis, Canthocalanus pauper, Subeu- and diversity 1.5 calanus subcrassus, Temora turbinata and Undinula vul- Indices of richness 0.6

Pielou's evenness index garis—all having a 100% occurrence rate (OR). Fifteen

1.0 0.5 copepod species were exclusively identified from a single 12345678 sample (OR = 12.5%). Of all the samples, the top five Sampling station abundant species were: Temora turbinata (relative abun- dance of 23.50%), Undinula vulgaris (17.92%), Acrocal- Fig. 6 Copepods recorded at stations 1–8; a copepod density and species number; b richness, evenness and Shannon-Wiener diversity anus gibber (14.73%), Canthocalanus pauper (11.49%) index and Acrocalanus gracilis (7.40%). The total numbers of the 123 Helgol Mar Res (2012) 66:621–634 629

Station 8 is separated from the others and allocated to group IA. The top three dominant copepod species of group IA were: Canthocalanus pauper (31.93%), Acrocalanus gracilis (26.99%) and Temora turbinata (11.09%). At the next grouping level, station 1 was separated as group IIA, which showed the lowest richness index (Fig. 6b) and a specific composition of copepod species. The top three dominant species of group IIA were: Temora turbinata (32.76%), Canthocalanus pauper (19.83%), and Acrocal- anus gibber (10.34%). In group IIA, two copepods, Temora turbinata (32.76%) and Centropages furcatus (6.90%) showed a higher proportion than in other cluster groups, and 7 species with relative abundances higher than 5%. The third level (III) separated the remaining stations into two groups. Group IIIA (stations 2, 4 and 5) were closer to land than the stations of group IIIB (stations 3, 6 and 7). The three most dominant species of group IIIA were: Temora turbinata (25.05%), Undinula vulgaris (22.61%) and Acrocalanus gibber (20.47%). The most dominant species of group IIIB were: Undinula vulgaris (17.89%), Temora turbinata (13.92%) and Canthocalanus pauper Fig. 7 Dendrogram indicating similarities between stations based on (13.02%). The copepods Subeucalanus subcrassus Bray–Curtis indexes for plankton composition (10.85%) and (5.35%) showed a higher abundance in group IIIB than in other groups. The results suggest that during the monsoon transition period copepod top five most abundant species contributed 75.04% to the communities in the surface waters of northern Taiwan vary total adundance of all samples (Table 3). Among all sam- horizontally and with distance to land. ples, the relative abundance of the indicator species Cal- anus sinicus was 0.65%, with an occurrence rate of 50.0%, Correlations with environmental factors and an average density for the 8 sampling stations of 3.37 ± 5.72 individuals m-3 (Table 3). Among all mesozooplankton taxa, the abundance of chaetognaths was negatively correlated with salinity (r = Cluster analysis 0.77, p = 0.027, Pearson’s correlation, Fig. 8a). In con- trast, the group number of the mesozooplankton showed a The dendrogram (Fig. 7) shows the results of a clustering positive correlation with salinity (r = 0.71, p = 0.048, analysis based on Bray-Curtis similarities to characterize Pearson’s correlation, Fig. 8b). The abundance of Acro- the copepod communities at the 8 sampling stations during calanus monachus (r = 0.75, p = 0.03, Pearson’s corre- the monsoon transition period. The values of IndVal were lation, Fig. 8c) and copepod species number (r = 0.91, calculated for copepods with relative abundances above p = 0.002, Pearson’s correlation, Fig. 8d) were also posi- 5% (Table 4). tively correlated with salinity. Species numbers increased

Table 4 Indicator value indexes of copepod species with more than 50% OR (indicator species) No. Indicator species (index value %) I A II A III A III B

1 Canthocalanus pauper (31.93) Temora turbinata (32.76) Temora turbinata (25.05) Undinula vulgaris (17.89) 2 Acrocalanus gracilis (26.99) Canthocalanus pauper (19.83) Undinula vulgaris (22.61) Temora turbinata (13.92) 3 Temora turbinata (11.09) Acrocalanus gibber (10.34) Acrocalanus gibber (20.47) Canthocalanus pauper (13.02) 4 Undinula vulgaris (9.95) Temora discaudata (9.05) Canthocalanus pauper (6.79) Subeucalanus subcrassus (10.85) 5 Centropages furcatus (6.90) Acrocalanus gracilis (6.24) Acrocalanus gracilis (10.62) 6 Undinula vulgaris (5.17) Acrocalanus gibber (6.17) 7 Calanopia minor (5.17) Oncaea venusta (5.35)

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200 correlation, Fig. 9e) and Labidocera acuta (r =-0.82, (a) Chaetognatha ) 160 p = 0.013, Pearson’s correlation, Fig. 9f).

-3 r = 0.77, p = 0.027

120

80 Discussion Density

(Individuals m 40 Zooplankton communities in the ocean are influenced by 0 several factors including river discharge (Tan et al. 2004), 25 monsoons (Yoshida et al. 2006), urban runoffs and change (b) Group number 20 r = 0.71, p = 0.048 of water masses (Tseng et al. 2008a). Tan et al. (2004) and Yoshida et al. (2006) reported copepods as the main frac- 15 tion of mesozooplankton in the Pearl River estuary and the 10 Malacca Strait, respectively. In the present study the dominant taxa of mesozooplankton were calanoid cope-

group number 5

Mesozooplankton pods (66.36%), followed by chaetognaths (9.44%). Huang 0 (1983) studied the zooplankton communities in the 5 upwelling waters off the southeastern coast of Taiwan, and (c) Acrocalanus monachus ) 4 reported calanoid copepods to be highly abundant -3 r = 0.75, p = 0.03 (44.0–59.7%) in all samples. Tseng et al. (2008a) found 3 calanoid copepods to dominate (37.07%) the mesozoo- 2

Density plankton communities in an outfall area in the northeastern South China Sea. The results confirm calanoid copepods to

(Individuals m 1 be the dominant mesozooplankton taxon. 0 Another dominant species in the present study was the 40 chaetognath Flaccisagitta enflata. This species is widely (d) Species number 35 r = 0.91, p = 0.002 distributed in the coastal waters of mainland China (Chen 30 1992). Chen (1992) reported the the species to be abundant 25 during summer and autumn in the waters of the boundary 20 zone of the Yellow Sea and the ECS. According to Pierrot- Copepod Bults and Nair (1991), the species is circum-globally dis-

species number 15 tributed and commonly found between 40oN and 40oS. Tse 10 33.3 33.6 33.9 34.2 et al. (2008) found F. enflata to be a dominant species in 0 the waters of Hong Kong. Tseng et al. (2011) reported the Salinity ( / ) 00 species to be abundant in the waters of the western and Fig. 8 Correlation between salinity and chaetognath density (a), southern ECS during a summer cruise. The present study number of mesozooplankton groups (b), densitiy of the copepod confirmed F. enflata to be abundant in the southern ECS Acrocalanus monachus (c), and number of copepod species (d), during the SW-NE monsoon transition period. The showing significant correlations (Pearson’s correlation analysis) amphipods Hyperioides sibaginis and Lestigonus bengal- ensis were common in the samples of the present study. H. sibaginis is distributed in the waters of eastern mainland with increasing distance of the sampling stations from the China and has been reported in the South China Sea (Chen coast. 1983; Lowry 2000), the Taiwan Strait (Lin and Chen Only a few mesozooplankton taxa showed changes in 1988), and the ECS (Xu and Jiang 2006;Xu2009). Our density which were significantly correlated with seawater study shows that this species can occur in the southern ECS temperature. The abundances of mesozooplanktonic during the monsoon transition period. amphipods (r =-0.79, p = 0.019, Pearson’s correlation, Copepod communities change dynamically with water Fig. 9a) and decapods (r =-0.81, p = 0.014, Pearson’s masses during northeast and southwest monsoons (Hsieh correlation, Fig. 9b) were negatively correlated with sea- et al. 2004, 2005; Hwang et al. 2004, 2006, 2009; Dur et al. water temperature, and this also applied to the following 2007; Tseng et al. 2008b). The dominant copepod species four copepod species: Calanus sinicus (r =-0.85, p = in the present study were: Temora turbinata, Undinula 0.008, Pearson’s correlation, Fig. 9c), Calocalanus pavo vulgaris, Acrocalanus gibber, Canthocalanus pauper and (r =-0.74, p = 0.035, Pearson’s correlation, Fig. 9d), Acrocalanus gracilis. These species are warm-water spe- Calanopia elliptica (r =-0.72, p = 0.044, Pearson’s cies that are commonly found around Taiwan (Shih and 123 Helgol Mar Res (2012) 66:621–634 631

Fig. 9 Correlation between 180 10.0 seawater temperature and the (a) Amphipoda (d) Calocalanus pavo densities of amphipods (a), 135 r = -0.79, p = 0.019 7.5 r = -0.74, p = 0.035 decapods (b), and the copepods Calanus sinicus (c), Calocalanus pavo (d), 90 5.0 Calanopia elliptica (e) and Labidocera acuta (f), showing 45 2.5 significant correlations (Pearson’s correlation analysis) 0 0.0 200 40 ) ) -3 (b) Other decapoda -3 (e) Calanopia elliptica 150 r = -0.81, p = 0.014 30 r = -0.72, p = 0.044

100 20

50 10 Density (Individuals m Density 0 Density (Individuals m 0 20 60 (c) Calanus sinicus (f) Labidocera acuta 15 r = -0.85, p = 0.008 45 r = -0.82, p = 0.013

10 30

5 15

0 0 26.5 27.0 27.5 28.0 28.5 29.0 26.5 27.0 27.5 28.0 28.5 29.0 Seawater temperature (oC)

Young 1995; Hwang et al. 2004; Dur et al. 2007; Tseng To date, there is no information on when C. sinicus first et al. 2008d, 2011b). Temora turbinata is an indicator arrives in the waters of northern Taiwan from its probable species of warm water masses (Dur et al. 2007; Tseng et al. origin in the Bohai Sea. Our results show that C. sinicus 2008b) which can also tolerate polluted environments was present in the sampling area in September 1998, before (Fang et al. 2006; Tseng et al. 2008e; Wu et al. 2010). the CCC affected the coastal areas of northern Taiwan. A limited number of studies reported a seasonal suc- This is clearly shown by the contemporaneous satellite cession of copepods in the waters north of Taiwan (Hwang images of the sea surface temperature (Fig. 2), indicating et al. 2004, 2006; Hwang and Wong 2005; Dur et al. 2007; that the colder waters of the CCC were still separated from Tseng et al. 2008b). These studies included different types the study area. Contrary to previous studies (Hwang et al. of coastal areas, including areas such as those close to 2004, 2006; Hwang and Wong 2005; Dur et al. 2007; nuclear power plants (Hwang et al. 2004), the estuary of Tseng et al. 2008b) that suggest C. sinicus to be exclusively the Danshuei River (Dur et al. 2007; Hwang et al. 2006, transported by the cold CCC water, we demonstrate that 2009), and the northeastern Taiwan Strait (Tseng et al. C. sinicus is present in the southern ECS even during the 2008b). Previous reports indicated that the calanoid cope- northeast monsoon transit period. However, it cannot be pod C. sinicus belongs to the cold-water masses of the CCC excluded that C. sinicus survives in the deeper layers of the that derive from the Yellow Sea during the northeast ECS when surface waters seasonally warm up, sinking to monsoon. Previous reports never found C. sinicus in deeper water during summer and returning to surface summer samples from the coastal areas. However, this waters via cold upwelling or vertical migration. species was frequently recorded with high rates of occur- Previous field studies reported C. sinicus in the south rence and relative abundance from October to April. Pre- ECS close to the present area of study. Hsieh et al. (2004) vious reports did not provide information about copepod still reported C. sinicus north of the Taiwan Strait when the composition in the waters north of Taiwan in September. northeast monsoon was prevailing. Liao et al. (2006) found This may be due to a lack of data collection in September. C. sinicus occurred in August at the upwelling area of the

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Table 5 Number of copepod Area of ECS Number of Study period References species identified in different identified parts and during different species periods in the East China Sea (ECS) Southwestern (Tanshui) 83 June/1970 Tseng (1975) Southwestern (Tanshui River estuary) 62 August/1996–January/ Hsieh and Chiu 1997 (1997) Southern (Coastal water) 25a May/1996 Hwang et al. (1998) Southern (Nuclear power plants) 37a August/1996 Wong et al. (1998) Southern (North of Taiwan) 113 April/1995 Shih and Chiu (1998) Southern (North of Taiwan) 183 March/1995 Shih et al. (2000) Southeastern (Upwelling water) 178 March/1995 Lo et al. (2004b) Southern (Nuclear power plants) 116 November/2000–December/ Hwang et al. (2004) 2003 Southwestern (Boundary coastal 110 October/1998–September/ Hwang et al. (2006) waters) 2003 Southeastern (Upwelling water) 95 August/1998 Liao et al. (2006) Southwestern (Estuary of Danshuei 79a October/1998–July/ Dur et al. (2007) River) 2004 Southwestern area 77 July/2001 Tseng et al. (2008d) Southwestern (Estuary of Danshuei 120 October/1998–July/ Hwang et al. (2009) River) 2004 a Only calanoid copepods Southern area 49 September/1998 Present study recorded southeastern ECS. Their study indicated that C. sinicus Chiu (1998) recorded 113 species in the upper 200 m. To occasionally occurred at low abundances. They suggested date, most ecological studies of copepod communities were that C. sinicus was coming from the north of the Taiwan performed in the southwestern ECS and the estuary of the Strait with the Taiwan Strait warm current. Chen (1992) Danshuei River (Tseng 1975; Hwang et al. 2006, 2009; Dur reported that the temperature range of C. sinicus was et al. 2007). This includes a longer study period of 6 years 5–23°C. Therefore, Liao et al. (2006) inferred that (Hwang et al. 2009). Hwang et al. (2004) identified 116 C. sinicus in fact comes from the waters of the northern copepod species during a 3-year study close to the nuclear Taiwan Strait and later appears at the surface due to power plants I and II in the northeastern coastal area of upwelling. In the present study we found three more spe- Taiwan, and 120 species were reported off the Danshui cies related to cold-water masses: Calocalanus pavo, Estuary during a 6-year study (Hwang et al. 2009). The Calanopia elliptica and Labidocera acuta, which are previous studies showed that the number of identified temperate species originating from the ECS (Chen 1992). copepod species increased with the temporal and spatial The copepod species numbers found in the southern scale of the investigations. ECS varied in different studies according to sampling The present study was carried out during the monsoonal location and study period (Table 5). The two studied areas transition period before the onset of the northeast monsoon with high species numbers were located in the upwelling in late summer. The SST image did not provide any evi- zone (Shih et al. 2000; Lo et al. 2004b; Liao et al. 2006) dence that the coastal areas of northern Taiwan were and in the southwest ECS in the estuary of Danshuei River affected by the CCC during the study period. Nevertheless, (Hwang et al. 2009). Upwelling areas with higher primary we identified C. sinicus in northern Taiwan waters. Future productivity commonly support a higher biodiversity of studies should focus on the deeper water layers of the ECS secondary producers (Nybakken 1993). Liao et al. (2006) to see whether C. sinicus uses the cold water stratum as a reported 95 species in the upwelling waters of the southeast refuge during the seasons with warm surface waters. ECS with higher species richness than previously reported from coastal areas (Hwang et al. 1998; Wong et al. 1998). Acknowledgments We thank Mr. Hsuan-Chan Wang for his Station 5 of the present study was located close to the assistance in the field work. Particular acknowledgement is given to the Department of Atmospheric Science at the National Taiwan upwelling area and showed the highest density of meso- University for providing us with the weather information (data bank zooplankton of the 8 sampling stations. Shih et al. (2000) for atmospheric research). We are thankful to anonymous reviewer and Lo et al. (2004b) found 178 and 183 species, respec- and editor, whose comments and suggestions substantially improved tively, in the upper 250 m water layer. Similarly, Shih and the manuscript.

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